Herptile gut microbiomes: a natural system to study multi-kingdom interactions between filamentous fungi and bacteria

• Published in: mSphere Vol. 9; no. 3; p. e0047523
• Main Authors: Vargas-Gastélum, Lluvia, Romer, Alexander S, Ghotbi, Marjan, Dallas, Jason W, Alexander, N Reed, Moe, Kylie C, McPhail, Kerry L, Neuhaus, George F, Shadmani, Leila, Spatafora, Joseph W, Stajich, Jason E, Tabima, Javier F, Walker, Donald M
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 26-03-2024
• Subjects: amphibian; anaerobic gut fungi; Bacteria; Basidiobolus; Biodiversity; Climate change; Conservation; cyclic peptide; Endangered species; Frogs; Fungi; Gene transfer; Genomes; Geography; Herpetofauna; Horizontal transfer; Host-Microbial Interactions; Intestinal microflora; Metabolism; Metabolites; Microbiomes; mycobiome; Phenotypes; Quality control; reptile; Reptiles & amphibians; Research Article; Sampling; specialized metabolite; Structure-function relationships; Taxonomy; Threatened species; Wildlife conservation; North Carolina; United States > US; Tennessee; Louisiana; Ohio; Georgia; Alabama; Arkansas; Arizona; mycobiome; anaerobic gut fungi; non-ribosomal peptide synthetases; cyclic peptide; reptile; amphibian; specialized metabolite
• ISSN: 2379-5042; 2379-5042
• DOI: 10.1128/msphere.00475-23

Reptiles and amphibians (herptiles) are some of the most endangered and threatened species on the planet and numerous conservation strategies are being implemented with the goal of ensuring species recovery. Little is known, however, about the gut microbiome of wild herptiles and how it relates to the health of these populations. Here, we report results from the gut microbiome characterization of both a broad survey of herptiles, and the correlation between the fungus
, and the bacterial community supported by a deeper, more intensive sampling of
, known as slimy salamanders. We demonstrate that bacterial communities sampled from frogs, lizards, and salamanders are structured by the host taxonomy and that
is a common and natural component of these wild gut microbiomes. Intensive sampling of multiple hosts across the ecoregions of Tennessee revealed that geography and host:geography interactions are strong predictors of distinct
operational taxonomic units present within a given host. Co-occurrence analyses of
and bacterial community diversity support a correlation and interaction between
and bacteria, suggesting that
may play a role in structuring the bacterial community. We further the hypothesis that this interaction is advanced by unique specialized metabolism originating from horizontal gene transfer from bacteria to
and demonstrate that
is capable of producing a diversity of specialized metabolites including small cyclic peptides.IMPORTANCEThis work significantly advances our understanding of biodiversity and microbial interactions in herptile microbiomes, the role that fungi play as a structural and functional members of herptile gut microbiomes, and the chemical functions that structure microbiome phenotypes. We also provide an important observational system of how the gut microbiome represents a unique environment that selects for novel metabolic functions through horizontal gene transfer between fungi and bacteria. Such studies are needed to better understand the complexity of gut microbiomes in nature and will inform conservation strategies for threatened species of herpetofauna.